Increased host tolerance of multiple cuckoo eggs leads to higher fledging success of the brood parasite

Animal Behaviour

Volumn 77, Issue 5, 2009, Pages 1281-1290

  Moskát, Csaba ^a   Hauber, Márk E ^b   Avilés, Jesús M ^c   Bán, Miklós ^d   Hargitai, Rita ^e,f   Honza, Marcel ^g  

^a INSTITUTE OF EXPERIMENTAL MEDICINE   (Hungary)

^b CITY UNIVERSITY OF NEW YORK   (United States)

^c UNIVERSITY OF GRANADA   (Spain)

^d UNIVERSITY OF DEBRECEN   (Hungary)

^e EÖTVÖS LORÁND UNIVERSITY   (Hungary)

^f Department of Agricultural Sciences and Environmental Management   (Hungary)

^g INSTITUTE OF VERTEBRATE BIOLOGY   (Czech Republic)

Author keywords

brood parasitism; common cuckoo; Cuculus canorus; egg recognition; egg rejection; evictor chick; mimicry; reproductive success

Indexed keywords

BIRD; BROOD PARASITISM; COGNITION; FLEDGING; HOST-PARASITE INTERACTION; MEMORY; MIMICRY; MORPHOLOGY; RECOGNITION; REPRODUCTIVE PRODUCTIVITY;

CENTRAL EUROPE; EURASIA; EUROPE; HUNGARY;

ACROCEPHALUS ARUNDINACEUS; AVES; CUCULIDAE; CUCULUS CANORUS;

EID: 64549150930     PISSN: 00033472     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.anbehav.2009.01.030     Document Type: Article

References (105)

1. Anderson M.G., and Hauber M.E. A recognition-free mechanism for reliable rejection of brood parasites. Trends in Ecology & Evolution 22 (2007) 283-286
2. Antonov A., Stokke B.G., Moksnes A., and Røskaft E. Egg rejection in marsh warblers (Acrocephalus palustris) heavily parasitized by common cuckoos (Cuculus canorus). Auk 123 (2006) 419-430
3. Antonov A., Stokke B.G., Moksnes A., and Røskaft E. First evidence of regular common cuckoo Cuculus canorus, parasitism on eastern olivaceous warblers, Hippolais pallida elaeica. Naturwissenschaften 94 (2007) 307-312
4. Avilés J.M., and Møller A.P. Meadow pipit (Anthus pratensis) egg appearance in cuckoo (Cuculus canorus) sympatric and allopatric populations. Biological Journal of the Linnean Society 79 (2003) 543-549
5. Avilés J.M., Rutila J., and Møller A.P. Should the redstart (Phoenicurus phoenicurus) accept or reject cuckoo eggs?. Behavioral Ecology and Sociobiology 58 (2005) 608-617
6. Baker E.C.S. Cuckoo Problems (1942), Witherby, London
7. Barabás L., Gilicze B., Takasu F., and Moskát C. Survival and anti-parasite defense in a host metapopulation under heavy brood parasitism: a source-sink dynamic model. Journal of Ethology 22 (2004) 143-151
8. Bártol I., Karcza Z., Moskát C., Røskaft E., and Kisbenedek T. Responses of great reed warblers Acrocephalus arundinaceus to experimental brood parasitism: the effects of a cuckoo Cuculus canorus dummy and egg mimicry. Journal of Avian Biology 33 (2002) 420-425
9. Brooke M.d.L., Davies N.B., and Noble D.G. Rapid decline of host defences in response to reduced cuckoo parasitism: behavioural flexibility of reed warblers in a changing world. Proceedings of the Royal Society of London, Series B 265 (1998) 1277-1282
10. Brooker L.C., and Brooker M.G. Why do splendid fairy-wrens always accept cuckoo eggs?. (Forum Debate). Behavioral Ecology 9 (1998) 419-424
11. Brooker L.C., Brooker M.G., and Brooker A.M.H. An alternative population-genetics model for the evolution of egg mimesis and egg crypsis in cuckoos. Journal of Theoretical Biology 146 (1990) 123-143
12. Cherry M.I., Bennett A.T.D., and Moskát C. Host intra-clutch variation, cuckoo egg matching and egg rejection by great reed warblers. Naturwissenschaften 94 (2007) 441-447
13. Cherry M.I., Bennett A.T.D., and Moskát C. Do cuckoos choose nests of great reed warblers on the basis of host egg appearance?. Journal of Evolutionary Biology 20 (2007) 1218-1222
14. Davies N.B. Cuckoos, Cowbirds and Other Cheats (2000), T. & A. D. Poyser, London
15. Davies N.B., and Brooke M.d.L. Cuckoos versus reed warblers: adaptations and counteradaptations. Animal Behaviour 36 (1988) 262-284
16. Davies N.B., and Brooke M.d.L. An experimental study of co-evolution between the cuckoo, Cuculus canorus, and its hosts. II. Host egg markings, chick discrimination and general discussion. Journal of Animal Ecology 58 (1989) 225-236
17. Davies N.B., Brooke M.d.L., and Kacelnik A. Recognition errors and probability of parasitism determine whether reed warblers should accept or reject mimetic cuckoo eggs. Proceedings of the Royal Society of London, Series B 263 (1996) 925-931
18. Davies N.B., Butchart S.H.M., Burke T.A., Chaline N., and Stewart I.R.K. Reed warblers guard against cuckoos and cuckoldry. Animal Behaviour 65 (2003) 285-295
19. Dyrcz A., and Halupka K. Great reed warbler Acrocephalus arundinaceus and reed warbler Acrocephalus scirpaceus respond differently to cuckoo dummy. Journal of Ornithology 147 (2006) 649-652
20. Dyrcz A., and Halupka K. Why frequency of nest parasitism by the cuckoo differ considerably between two populations of warblers living in the same habitat?. Ethology 113 (2007) 209-213
21. Ellison K., Sealy S.G., and Gibbs H.L. Genetic elucidation of host use by individual sympatric bronzed cowbirds (Molothrus aeneus) and brown-headed cowbirds (M. ater). Canadian Journal of Zoology 84 (2006) 1269-1280
22. Garamszegi L.Z., and Avilés J.M. Brood parasitism by brown-headed cowbirds and the expression of sexual characters in their hosts. Oecologia 143 (2005) 167-177
23. Grim T. Why is mimicry in cuckoo eggs sometimes so poor?. Journal of Avian Biology 33 (2002) 302-305
24. Grim T. The evolution of nestling discrimination by hosts of parasitic birds: why is rejection so rare?. Evolutionary Ecology Research 8 (2006) 785-802
25. Grim T., Rutila J., Cassey P., and Hauber M.E. Experimentally constrained virulence is costly for common cuckoo Cuculus canorus chicks. Ethology 115 (2009) 14-22
26. Hauber M.E. Site selection and repeatability in brown-headed cowbird (Molothrus ater) parasitism of eastern phoebe (Sayornis phoebe) nests. Canadian Journal of Zoology 79 (2001) 1518-1523
27. Hauber M.E. Is reduced clutch size a cost of parental care in eastern phoebes (Sayornis phoebe)?. Behavioral Ecology and Sociobiology 51 (2002) 503-509
28. Hauber M.E. Lower begging responsiveness of host versus parasitic brown-headed cowbird (Molothrus ater) nestlings is related to species identity but not early social experience. Journal of Comparative Psychology 117 (2003) 24-30
29. Hauber M.E. A future cost of misdirected parental care for brood parasitic young?. Folia Zoologica 55 (2006) 367-374
30. Hauber M.E., and Kilner R.M. Coevolution, communication, and host-chick mimicry in parasitic finches: who mimics whom?. Behavioral Ecology and Sociobiology 61 (2007) 497-503
31. Hauber M.E., and Montenegro K. What are the costs of raising a brood parasite? Comparisons of host parental care at parasitized and non-parasitized broods. Etologia 10 (2002) 1-9
32. Hauber M.E., and Moskát C. Shared parental care is costly for nestlings of common cuckoos and their great reed warbler hosts. Behavioral Ecology 19 (2008) 79-86
33. Hauber M.E., and Sherman P.W. Self-referent phenotype matching: theoretical possibilities and empirical tests. Trends in Neurosciences 10 (2001) 609-616
34. Hauber M.E., Yeh P.J., and Roberts J.O.L. Patterns and coevolutionary consequences of repeated brood parasitism. Proceedings of the Royal Society of London, Series B 271 (2004) S317-S320
35. Hauber M.E., Moskát C., and Bán M. Experimental shift in hosts' acceptance threshold of inaccurate-mimic brood parasite eggs. Biology Letters 2 (2006) 177-180
36. Honza M., and Moskát C. Antiparasite behaviour in response to experimental brood parasitism in the great reed warbler: a comparison of single and multiple parasitism. Annales Zoologici Fennici 42 (2005) 627-633
37. Honza M., Picman J., Grim T., Novák V., Capek M., and Mrlík V. How to hatch from an egg of great strength. A study of the common cuckoo. Journal of Avian Biology 32 (2001) 249-255
38. Honza M., Sicha V., Procházka P., and Lezalová R. Host nest defense against a color-dimorphic brood parasite: great reed warblers (Acrocephalus arundinaceus) versus common cuckoos (Cuculus canorus). Journal of Ornithology 147 (2006) 629-637
39. Honza M., Voslajerová K., and Moskát C. Eviction behaviour of the common cuckoo Cuculus canorus chicks. Journal of Avian Biology 38 (2007) 385-389
40. Honza M., Pozgayová M., Procházka P., and Tkadlec E. Consistency in egg rejection behaviour: responses to repeated brood parasitism in the blackcap (Sylvia atricapilla). Ethology 113 (2007) 344-351
41. Honza M., Polaciková L., and Procházka P. Ultraviolet and green parts of the colour spectrum affect egg rejection in the song thrush (Turdus philomelos). Biological Journal of the Linnean Society 92 (2007) 269-276
42. Hoover J.P. Multiple effects of brood parasitism reduce the reproductive success of prothonotary warblers, Protonotaria citrea. Animal Behaviour 65 (2003) 923-934
43. Hoover J.P., Yasukawa K., and Hauber M.E. Spatially and temporally structured avian brood parasitism affects the fitness benefits of hosts' rejection strategies. Animal Behaviour 72 (2006) 881-890
44. Kilner R.M. The evolution of virulence in brood parasites. Ornithological Science 4 (2005) 55-64
45. Krüger O. Cuckoos, cowbirds and hosts: adaptations, trade-offs and constraints. Philosophical Transactions of the Royal Society of London, Series B 362 (2007) 1873-1886
46. Krüger O., and Davies N.B. The evolution of cuckoo parasitism: a comparative analysis. Proceedings of the Royal Society of London, Series B 269 (2002) 375-381
47. Krüger O., Davies N.B., and Sorenson M.D. The evolution of sexual dimorphism in parasitic cuckoos: sexual selection or coevolution?. Proceedings of the Royal Society of London, Series B 274 (2007) 1553-1560
48. Langmore N.E., Hunt S., and Kilner R.M. Escalation of a coevolutionary arms race through host rejection of brood parasitic young. Nature 122 (2003) 157-160
49. Lea S.E.G., and Kattan G.H. Reanalysis gives further support to the 'shotgun' model of shiny cowbird parasitism of house wren nests. Animal Behaviour 56 (1998) 1571-1573
50. Lotem A., Nakamura H., and Zahavi A. Rejection of cuckoo eggs in relation to host age: a possible evolutionary equilibrium. Behavioral Ecology 3 (1992) 128-132
51. Lotem A., Nakamura H., and Zahavi A. Constraints on egg discrimination and cuckoo-host co-evolution. Animal Behaviour 49 (1995) 1185-1209
52. Lovászi P., and Moskát C. Break-down of arms race between the red-backed shrike (Lanius collurio) and common cuckoo (Cuculus canorus). Behaviour 141 (2004) 245-262
53. McLaren C.M., Woolfenden B.E., Gibbs H.L., and Sealy S.G. Genetic and temporal patterns of multiple parasitism by brown-headed cowbirds (Molothrus ater) on song sparrows (Melospiza melodia). Canadian Journal of Zoology 81 (2003) 281-286
54. Marchetti K. Egg rejection in a passerine bird: size does matter. Animal Behaviour 59 (2000) 877-883
55. Marchetti K., Nakamura H., and Gibbs H.L. Host-race formation in the common cuckoo. Science 282 (1998) 471-472
56. Martín-Gálvez D., Soler J.J., Martínez J.G., Krupa A.P., Richard M., Soler M., Møller A.P., and Burke T. A quantitative trait locus for recognition of foreign eggs in the host of a brood parasite. Journal of Evolutionary Biology 19 (2006) 543-550
57. Martínez J.G., Soler J.J., Soler M., and Burke T. Spatial pattern of egg laying and multiple parasitism in a brood parasite: a non-territorial system in the great spotted cuckoo (Clamator glandarius). Oecologia 117 (1998) 286-294
58. Moksnes A. Egg recognition in chaffinches and bramblings. Animal Behaviour 44 (1992) 993-995
59. Moksnes A., and Røskaft E. Egg-morphs and host preference in the common cuckoo Cuculus canorus: an analysis of cuckoo and host eggs from European museum collections. Journal of Zoology 236 (1995) 625-648
60. Moksnes A., Røskaft E., Braa A.T., Korsnes L., Lampe H.M., and Pedersen H.C. Behavioural responses of potential hosts towards artificial cuckoo eggs and dummies. Behaviour 116 (1991) 64-89
61. Moksnes A., Røskaft E., Bicik V., Honza M., and Øien I.J. Cuckoo Cuculus canorus parasitism on Acrocephalus warblers in Southern Moravia in the Czech Republic. Journal für Ornithologie 134 (1993) 425-434
62. Moksnes A., Røskaft E., Rudolfsen G., Skjelseth S., Stokke B.G., Kleven O., Gibbs H.L., Honza M., Taborsky B., Teuschl Y., Vogl W., and Taborsky M. Individual female common cuckoos Cuculus canorus lay constant egg types but egg appearance cannot be used to assign eggs to females. Journal of Avian Biology 39 (2008) 238-241
63. Molnár B. The cuckoo in the Hungarian plain. Aquila 51 (1944) 100-112
64. Moskát C. Nest defence and egg rejection in great reed warblers over the breeding cycle: are they synchronised with the risk of brood parasitism?. Annales Zoologici Fennici 42 (2005) 579-586
65. Moskát C., and Hauber M.E. Conflict between egg recognition and rejection decisions in common cuckoo (Cuculus canorus) hosts. Animal Cognition 10 (2007) 377-386
66. Moskát C., and Honza M. European cuckoo Cuculus canorus parasitism and host's rejection behaviour in a heavily parasitized great reed warbler Acrocephalus arundinaceus population. Ibis 144 (2002) 614-622
67. Moskát C., Szentpéteri J., and Barta Z. Adaptations by great reed warblers to brood parasitism: a comparison of populations in sympatry and allopatry with the common cuckoo. Behaviour 139 (2002) 1313-1329
68. Moskát C., Barta Z., Hauber M.E., and Honza M. High synchrony of egg laying in common cuckoos (Cuculus canorus) and their great reed warbler (Acrocephalus arundinaceus) hosts. Ethology Ecology and Evolution 18 (2006) 57-65
69. Moskát C., Avilés J.M., Bán M., Hargitai R., and Zölei A. Experimental support for the use of egg uniformity in parasite egg discrimination by cuckoo hosts. Behavioral Ecology and Sociobiology 62 (2008) 1885-1890
70. Moskát C., Hansson B., Barabás L., Bártol I., and Karcza Z. Common cuckoo Cuculus canorus parasitism, antiparasite defence and gene flow in closely located populations of great reed warblers Acrocephalus arundinaceus. Journal of Avian Biology 39 (2008) 663-671
71. Moskát C., Székely T., Cuthill I.C., and Kisbenedek T. Hosts' responses to parasitic eggs: which cues elicit hosts' egg discrimination?. Ethology 114 (2008) 186-194
72. Øien I.J., Moksnes A., and Røskaft E. Evolution of variation in egg color and marking pattern in European passerines: adaptations in a coevolutionary arms race with the cuckoo, Cuculus canorus. Behavioral Ecology 6 (1995) 166-174
73. Øien I.J., Moksnes A., Røskaft E., and Honza M. Costs of cuckoo Cuculus canorus parasitism to reed warblers Acrocephalus scirpaceus. Journal of Avian Biology 29 (1998) 209-215
74. Parejo D., and Avilés J.M. Do avian brood parasites eavesdrop on heterospecific sexual signals, revealing host quality? A review of the evidence. Animal Cognition 10 (2007) 81-88
75. Payne R.B., and Payne L.L. Brood parasitism by cowbirds: risks and effects on reproductive success and survival in indigo buntings. Behavioral Ecology 9 (1998) 64-73
76. Payne R.B., Woods J.L., and Payne L.L. Parental care in estrilid finches: experimental tests of a model of Vidua brood parasitism. Animal Behaviour 62 (2001) 473-483
77. Reeve H.K. The evolution of conspecific acceptance thresholds. American Naturalist 133 (1989) 407-435
78. Rodríguez-Gironés M.A., and Lotem A. How to detect a cuckoo egg: a signal-detection theory model for recognition and learning. American Naturalist 153 (1999) 633-648
79. Røskaft E., Moksnes A., Stokke B.G., Bicik V., and Moskát C. Aggression to dummy cuckoos by potential European cuckoo hosts. Behaviour 139 (2002) 613-628
80. Røskaft E., Moksnes A., Stokke B.G., Moskát C., and Honza M. The spatial habitat structure of host populations explains the pattern of rejection behavior in hosts and parasitic adaptations in cuckoos. Behavioral Ecology 13 (2002) 163-168
81. Røskaft E., Takasu F., Moksnes A., and Stokke B.G. Importance of spatial habitat structure on establishment of host defenses against brood parasitism. Behavioral Ecology 17 (2006) 700-708
82. Rothstein S.I. Mechanisms of avian egg recognition: possible learned and innate factors. Auk 91 (1974) 796-807
83. Rothstein S.I. Evolutionary rates and host defenses against avian brood parasitism. American Naturalist 109 (1975) 161-176
84. Rothstein S.I. Mechanisms of avian egg recognition: do birds know their own eggs?. Animal Behaviour 23 (1975) 268-278
85. Rothstein S.I. Successes and failures in avian egg and nestling recognition with comments on the utility of optimal reasoning. American Zoologist 22 (1982) 547-560
86. Rutila J., Latja R., and Koskela K. The common cuckoo Cuculus canorus and its cavity nesting hosts, the redstart Phoenicurus phoenicurus: a peculiar cuckoo-host system. Journal of Avian Biology 33 (2002) 414-419
87. Schuetz J.G. Low survival of parasite chicks may result from their imperfect adaptation to hosts rather than expression of defenses against parasitism. Evolution 59 (2005) 2017-2024
88. Schulze-Hagen K. Parasitism and egg losses due to the cuckoo (Cuculus canorus) in reed and marsh warblers (Acrocephalus scirpaceus, A. palustris) in central and western Europe. Journal für Ornithologie 133 (1992) 237-249
89. Schulze-Hagen K., Stokke B.G., and Birkhead T. Reproductive biology of the European cuckoo Cuculus canorus: early insights, persistent errors and the acquisition of knowledge. Journal of Ornithology 150 (2009) 1-16
90. Servedio M.R., and Hauber M.E. To eject or to abandon? Life history traits of hosts and parasites interact to influence the fitness payoffs of alternative anti-parasite strategies. Journal of Evolutionary Biology 19 (2006) 1585-1594
91. Servedio M.R., and Lande R. Coevolution of an avian host and its parasitic cuckoo. Evolution 57 (2003) 1164-1175
92. Soler J.J., and Møller A.P. A comparative analysis of the evolution of variation in appearance of eggs of European passerines in relation to brood parasitism. Behavioral Ecology 7 (1996) 89-94
93. Soler M., and Møller A.P. Duration of sympatry and coevolution between the great spotted cuckoo and its magpie host. Nature 343 (1990) 748-750
94. Soler M., and Soler J.J. Innate versus learned recognition of conspecifics in great spotted cuckoos Clamator glandarius. Animal Cognition 2 (1999) 97-102
95. Southern H.N. Mimicry in cuckoo eggs. In: Huxley J., Hardy A.C., and Ford E.B. (Eds). Evolution as a Process (1954), George, Allen & Unwin, London 219-232
96. Stokke B.G., Moksnes A., Røskaft E., Rudolfsen G., and Honza M. Rejection of artificial cuckoo (Cuculus canorus) eggs in relation to variation in egg appearance among reed warblers (Acrocephalus scirpaceus). Proceedings of the Royal Society of London, Series B 266 (1999) 1483-1488
97. Stokke B.G., Honza M., Moksnes A., Røskaft E., and Rudolfsen G. Costs associated with recognition and rejection of parasitic eggs in two European passerines. Behaviour 139 (2002) 629-644
98. Stokke B.G., Hafstad I., Rudolfsen G., Bargain B., Beier J., Campas D.B., Dyrcz A., Honza M., Leisler B., Pap P.L., Patavicius R., Procházka P., Schulze-Hagen K., Thomas R., Moksnes A., Møller A.P., Røskaft E., and Soler M. Host density predicts presence of cuckoo parasitism in reed warblers. Oikos 116 (2007) 913-922
99. Stokke B.G., Takasu F., Moksnes A., and Røskaft E. The importance of clutch characteristics for antiparasite adaptations in hosts of avain brood parasites. Evolution 61 (2007) 2212-2228
100. Takasu F., Kawasaki K., Nakamura H., Cohen J.E., and Shigesada N. Modeling the population dynamics of a cuckoo-host association and the evolution of host defenses. American Naturalist 142 (1993) 819-839
101. Tonra C.M., Hauber M.E., Heath S.K., and Johnson M.D. Ecological correlates and sex differences in early development of a generalist brood parasite. Auk 125 (2008) 205-213
102. Török J., Moskát C., Michl G., and Péczely P. Common cuckoos (Cuculus canorus) lay eggs with larger yolk but not more testosterone than their great reed warbler (Acrocephalus arundinaceus) hosts. Ethology Ecology and Evolution 16 (2004) 271-277
103. Trine C.L. Effects of multiple parasitism on cowbird and wood thrush nesting success. In: Smith J.N.M., Cook T.L., Rothstein S.I., Robinson S.K., and Sealy S.G. (Eds). Ecology and Management of Cowbirds (2000), University of Texas Press, Austin 135-144
104. Tuero A.T., Fiorini V.D., and Reboreda J.C. Effects of shiny cowbird Molothrus bonariensis parasitism on different components of house wren Troglodytes aedon reproductive success. Ibis 149 (2007) 521-529
105. Wyllie I. The Cuckoo (1981), Batsford, London